Enhanced control of in vivo bone formation with surface functionalized alginate microbeads incorporating heparin and human bone morphogenetic protein-2

Tissue Engineering - Part A

Volumn 19, Issue 3-4, 2013, Pages 350-359

  Abbah, Sunny Akogwu ^a   Liu, Jing ^b   Goh, James Cho Hong ^a   Wong, Hee Kit ^a,c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c University Orthopaedics   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMECHANICS; COLLAGEN; COMPUTERIZED TOMOGRAPHY; PHOSPHATASES; POLYSACCHARIDES; STIFFNESS; STRONTIUM; THREE DIMENSIONAL COMPUTER GRAPHICS; TISSUE;

ALKALINE PHOSPHATASE ACTIVITY; BENDING STIFFNESS; BONE FORMATION; BONE REGENERATION; BONE TISSUE; BONE VOLUME FRACTION; BURST RELEASE; COLLAGEN SPONGE; CONTROL GROUPS; DELIVERY METHODS; FUNCTIONALIZED; HUMAN BONES; IN-VITRO EVALUATION; IN-VIVO; MICROBEADS; MICROCOMPUTED TOMOGRAPHY; RECOMBINANT HUMAN BONE MORPHOGENETIC PROTEIN-2 (RHBMP-2); RHBMP-2; SPINAL FUSION; SURFACE FUNCTIONALIZATION;

BONE;

RATTUS;

ALGINIC ACID; BMP2 PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN 2; GLUCURONIC ACID; HEPARIN; HEXURONIC ACID;

ANIMAL; ARTICLE; BONE REGENERATION; CHEMISTRY; DELAYED RELEASE FORMULATION; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; HUMAN; LUMBAR VERTEBRA; MALE; MICROCAPSULE; PATHOLOGY; PHYSIOLOGY; RAT; SPINE FRACTURE; SPRAGUE DAWLEY RAT; SYNTHESIS;

ALGINATES; ANIMALS; BONE MORPHOGENETIC PROTEIN 2; BONE REGENERATION; CAPSULES; DELAYED-ACTION PREPARATIONS; GLUCURONIC ACID; HEPARIN; HEXURONIC ACIDS; HUMANS; LUMBAR VERTEBRAE; MALE; RATS; RATS, SPRAGUE-DAWLEY; SPINAL FRACTURES;

MLCS; MLOWN;

EID: 84872112186     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2012.0274     Document Type: Article

References (46)

1. Reddi, A.H. Morphogenesis and tissue engineering of bone and cartilage: inductive signals, stem cells, and biomimetic biomaterials. Tissue Eng 6, 351, 2000.
2. Carragee, E.J., Hurwitz, E.L., and Weiner, B.K. A critical review of recombinant human bone morphogenetic protein-2 trials in spinal surgery: emerging safety concerns and lessons learned. Spine J 11, 471, 2011.
3. Lee, J.W., Lee, S., Lee, S.H., Yang, H.S., Im, G.I., Kim, C.S., et al. Improved spinal fusion efficacy by long-term delivery of bone morphogenetic protein-2 in a rabbit model. Acta Orthop 82, 756, 2011.
4. Khan, S.A., Nelson, M.S., Pan, C., Gaffney, P.M., and Gupta, P. Endogenous heparan sulfate and heparin modulate bone morphogenetic protein-4 signaling and activity. Am J Phy-siol Cell Physiol 294, 1387C, 2008.
5. Dejima, K., Kanai, M.I., Akiyama, T., Levings, D.C., and Nakato, H. Novel contact-dependent bone morphogenetic protein (BMP) signaling mediated by heparan sulfate pro-teoglycans. J Biol Chem 286, 17103, 2011.
6. Bramono, D.S., Murali, S., Rai, B., Ling, L., Poh, W.T., Lim, Z.X., et al. Bone marrow-derived heparan sulfate potentiates the osteogenic activity of bone morphogenetic protein-2 (BMP-2). Bone 50, 954, 2011.
7. Jeon, O., Krebs, M., and Alsberg, E. Controlled and sus-tained gene delivery from injectable, porous PLGA scaffolds. J Biomed Mater Res A 98, 72, 2011.
8. Jeon, O., Powell, C., Ahmed, S.M., and Alsberg, E. Biode-gradable, photocrosslinked alginate hydrogels with inde-pendently tailorable physical properties and cell adhesivity. Tissue Eng Part A 16, 2915, 2010.
9. Yang, H.S., La, W.G., Bhang, S.H., Jeon, J.Y., Lee, J.H., and Kim, B.S. Heparin-conjugated fibrin as an injectable system for sustained delivery of bone morphogenetic protein-2. Tissue Eng Part A 16, 1225, 2010.
10. Zhao, B., Katagiri, T., Toyoda, H., Takada, T., Yanai, T., Fukuda, T., et al. Heparin potentiates the in vivo ectopic bone formation induced by bone morphogenetic protein-2. J Biol Chem 281, 23246, 2006.
11. Xu, X., Jha, A.K., Duncan, R.L., and Jia, X. Heparin-deco-rated, hyaluronic acid-based hydrogel particles for the con-trolled release of bone morphogenetic protein 2. Acta Biomater 7, 3050, 2011.
12. Chu, H., Johnson, N.R., Mason, N.S., and Wang, Y. A [polycation:heparin] complex releases growth factors with enhanced bioactivity. J Control Release 150, 157, 2011.
13. Zern, B.J., Chu, H., and Wang, Y. Control growth factor release using a self-assembled [polycation:heparin] complex. PLoS One 5, e11017, 2010.
14. Rokstad, A.M., Brekke, O.L., Steinkjer, B., Ryan, L., Kollar-ikova, G., Strand, B.L., et al. Alginate microbeads are com-plement compatible, in contrast to polycation containing microcapsules, as revealed in a human whole blood model. Acta Biomater 7, 2566, 2011.
15. de Vos, P., Faas, M.M., Strand, B., and Calafiore, R. Alginate-based microcapsules for immunoisolation of pancreatic is-lets. Biomaterials 27, 5603, 2006.
16. Strand, B.L., Morch, Y.A., Espevik, T., and Skjak-Braek, G. Visualization of alginate-poly-L-lysine-alginate microcap-sules by confocal laser scanning microscopy. Biotechnol Bioeng 82, 386, 2003.
17. Varghese, M.S., Hildebrandt, D., Glasser, D., Rubin, D.M., and Crowther, N.J. The effect of poly-L-lysine/alginate bead membrane characteristics on the absorption of heparin. Artif Cells Blood Substit Immobil Biotechnol 37, 13, 2009.
18. Abbah, S.A., Lam, C.X., Hutmacher, D.W., Goh, J.C., and Wong, H.K. Biological performance of a polycaprolactone-based scaffold used as fusion cage device in a large animal model of spinal reconstructive surgery. Biomaterials 30, 5086, 2009.
19. Hoemann, C.D., El-Gabalawy, H., and McKee, M.D. In vitro osteogenesis assays: influence of the primary cell source on alkaline phosphatase activity and mineralization. Pathol Biol (Paris) 57, 318, 2009.
20. Abbah, S.A., Lam, C.X., Ramruttun, A.K., Goh, J.C., and Wong, H.K. Fusion performance of low dose rhbmp-2 and bmscs in biodegradable scaffolds: a comparative study in a large animal model of anterior lumbar interbody fusion. Spine (Phila Pa 1976) 36, 1752, 2011.
21. Morisue, H., Matsumoto, M., Chiba, K., Matsumoto, H., Toyama, Y., Aizawa, M., et al. A novel hydroxyapatite fiber mesh as a carrier for recombinant human bone morphogenetic protein-2 enhances bone union in rat pos-terolateral fusion model. Spine (Phila Pa 1976) 31, 1194, 2006.
22. Ziran, B.H., Pineda, S., Pokharna, H., Esteki, A., Mansour, J.M., and Moskowitz, R.W. Biomechanical, radiologic, and histopathologic correlations in the pathogenesis of experi-mental intervertebral disc disease. Spine (Phila Pa 1976) 19, 2159, 1994.
23. Arakawa, T., Wen, J., and Philo, J.S. Stoichiometry of hepa-rin binding to basic fibroblast growth factor. Arch Biochem Biophys 308, 267, 1994.
24. Fu, T.S., Chen, W.J., Chen, L.H., Lin, S.S., Liu, S.J., and Ueng, S.W. Enhancement of posterolateral lumbar spine fusion using low-dose rhBMP-2 and cultured marrow stromal cells. J Orthop Res 27, 380, 2009.
25. Rolny, C., Spillmann, D., Lindahl, U., and Claesson-Welsh, L. Heparin amplifies platelet-derived growth factor (PDGF)-BB-induced PDGF alpha -receptor but not PDGF beta -receptor tyrosine phosphorylation in heparan sulfate-deficient cells. Effects on signal transduction and biological responses. J Biol Chem 277, 19315, 2002.
26. Damon, D.H., Lobb, R.R., D'Amore, P.A., and Wagner, J.A. Heparin potentiates the action of acidic fibroblast growth factor by prolonging its biological half-life. J Cell Physiol 138, 221, 1989.
27. Zakrzewska, M., Wiedlocha, A., Szlachcic, A., Krowarsch, D., Otlewski, J., and Olsnes, S. Increased protein stability of FGF1 can compensate for its reduced affinity for heparin. J Biol Chem 284, 25388, 2009.
28. Hausser, H.J., and Brenner, R.E. Low doses and high doses of heparin have different effects on osteoblast-like Saos-2 cells in vitro. J Cell Biochem 91, 1062, 2004.
29. Kim, S.E., Song, S.H., Yun, Y.P., Choi, B.J., Kwon, I.K., Bae, M.S., et al. The effect of immobilization of heparin and bone morphogenic protein-2 (BMP-2) to titanium surfaces on in-flammation and osteoblast function Biomaterials 32,366,2011.
30. Johnson, M.R., Boerckel, J.D., Dupont, K.M., and Guldberg, R.E. Functional restoration of critically sized segmental de-fects with bone morphogenetic protein-2 and heparin treat-ment. Clin Orthop Relat Res 469, 3111,2011.
31. Lin, H., Zhao, Y., Sun, W., Chen, B., Zhang, J., Zhao, W., et al. The effect of crosslinking heparin to demineralized bone matrix on mechanical strength and specific binding to human bone morphogenetic protein-2. Biomaterials 29,1189, 2008.
32. Jeon, O., Powell, C., Solorio, L.D., Krebs, M.D., and Alsberg, E. Affinity-based growth factor delivery using biodegrad-able, photocrosslinked heparin-alginate hydrogels. J Control Release 154, 258, 2011.
33. Klimo, P., Jr., and Peelle, M.W. Use of polyetheretherketone spacer and recombinant human bone morphogenetic pro-tein-2 in the cervical spine: a radiographic analysis. Spine J 9, 959, 2009.
34. Carragee, E.J., Ghanayem, A.J., Weiner, B.K., Rothman, D.J., and Bono, C.M. A challenge to integrity in spine publica-tions: years of living dangerously with the promotion of bone growth factors. Spine J 11, 463, 2011.
35. Anderson, C.L., and Whitaker, M.C. Heterotopic ossification associated with recombinant human bone morphogenetic protein-2 (infuse) in posterolateral lumbar spine fusion: a case report. Spine (Phila Pa 1976) 37, E502, 2012.
36. Salisbury, E.A., Olmsted-Davis, E.A., and Davis, A.R. Ad-verse events and bone morphogenetic protein-2. Spine J 11, 802, 2011.
37. Crouzier, T., Szarpak, A., Boudou, T., Auzely-Velty, R., and Picart, C. Polysaccharide-blend multilayers containing hya-luronan and heparin as a delivery system for rhBMP-2. Small 6, 651, 2010.
38. Simmons, C.A., Alsberg, E., Hsiong, S., Kim, W.J., and Mooney, D.J. Dual growth factor delivery and controlled scaffold degradation enhance in vivo bone formation by transplanted bone marrow stromal cells. Bone 35, 562, 2004.
39. Kolambkar, Y.M., Dupont, K.M., Boerckel, J.D., Huebsch, N., Mooney, D.J., and Hutmacher, D.W., et al. An alginate-based hybrid system for growth factor delivery in the functional repair of large bone defects. Biomaterials 32, 65, 2011.
40. Kho, V.K., and Chen, W.C. Posterolateral fusion using la-minectomy bone chips in the treatment of lumbar spondy-lolisthesis. Int Orthop 32, 115, 2008.
41. Gazdag, A.R., Lane, J.M., Glaser, D., and Forster, R.A. Al-ternatives to Autogenous Bone Graft: Efficacy and Indica-tions. J Am Acad Orthop Surg 3, 1, 1995.
42. Ponnappan, R.K., Serhan, H., Zarda, B., Patel, R., Albert, T., and Vaccaro, A.R. Biomechanical evaluation and compari-son of polyetheretherketone rod system to traditional tita-nium rod fixation. Spine J 9, 263, 2009.
43. Dawson, E., Bae, H.W., Burkus, J.K., Stambough, J.L., and Glassman, S.D. Recombinant human bone morphogenetic protein-2 on an absorbable collagen sponge with an osteo-conductive bulking agent in posterolateral arthrodesis with instrumentation. A prospective randomized trial. J Bone Joint Surg Am 91, 1604, 2009.
44. Rao, R.D., Bagaria, V.B., and Cooley, B.C. Posterolateral in-tertransverse lumbar fusion in a mouse model: surgical anatomy and operative technique. Spine J 7, 61, 2007.
45. Sawyer, A.A., Song, S.J., Susanto, E., Chuan, P., Lam, C.X., Woodruff, M.A., et al. The stimulation of healing within a rat calvarial defect by mPCL-TCP/collagen scaffolds loaded with rhBMP-2. Biomaterials 30, 2479, 2009.
46. Abbah, S.A., Lam, C.X., Ramruttun, K.A., Goh, J.C., and Wong. H.K. Autogenous bone marrow stromal cell sheets-loaded mPCL/TCP scaffolds induced osteogenesis in a porcine model of spinal interbody fusion. Tissue Eng Part A 17, 809, 2011.